composite malignant tumour the elderly...

J. clin. Path., 1970,23, 414422

A composite malignant tumour of theelderly female breast

D. M. WAYTE, J. B. STEWART, AND C. G. McKENZIEFrom the Royal Army Medical College, Millbank, London, and the Military Hospital, Colchester, Essex

SYNOPSIS A composite malignant tumour arising in the breast of an elderly woman isdescribed. The cystic tumour containing areas of squamous metaplasia, bone formation,adenocarcinoma, and osteosarcoma was surrounded by the typical changes of mammarydysplasia (fibroadenosis).The classification and acceptance of such tumours is highly debatable. There is no one

acceptable classification of breast sarcomas and hence the prognosis of such neoplasms,particularly those containing heterologous tissues, is poorly defined. Evidence is presentedin support of such composite tumours as being definite entities which arise from the closelyassociated epithelial and mesenchymal components of the breast simultaneously.

Sarcoma of the human breast, particularly whenarising contiguously with an adenocarcinoma,remains a perplexing and controversial problemfor both the surgeon and the pathologist (Hilland Stout, 1942). The great rarity of such malig-nant tumours and the inability to predict possiblebehaviour from the microscopic appearancepartly account for the aura of scepticism whichattends the diagnosis of a combined sarcomaand adenocarcinoma (Tudhope, 1939). There isalways the doubt that the sarcomatous element issimply an undifferentiated spindle cell variant ofthe carcinoma (Stewart, 1950; Willis, 1958). Butit is clear that the difficulties concerning theinterpretation and acceptance of a combined orcomposite tumour can be accounted for by neglectof two basic features of mammary structure andpathology.

In the first instance it is well known that thereexists a unique relationship between the epithelialcomponent and its closely investing 'specialized'connective tissue. In the mammary dysplasia offibroadenosis and in the benign fibroadenomatasuch a relationship is clearly seen. It is thereforenot unreasonable to accept that on rare occasionsboth components may assume malignant changejointly and thereby produce the compositetumour. This argument is reinforced by the know-Received for publication 21 October 1969.

ledge that the great majority of such tumours andbreast sarcomas are considered to arise fromfibroadenomas (Curran and Dodge, 1962).The second feature that is often forgotten in

regard to breast pathology is the extraordinarytendency for sarcomas of the breast to undergometaplasia resulting in the formation of heterolo-gous tissues which include bone, cartilage, andtheir malignant counterparts (Jemstrom, Lind-berg, and Meland, 1963; Gonzalez-Licea, Yardley,and Hartmann, 1967).We report the present case because of the rarity

of the so-called mixed or composite tumours ofthe breast and to outline some of the controversythat exists concerning breast sarcomas. Thecomposite tumour reported here contained alarge squamous-epithelium-lined cyst, areas ofbone metaplasia, and an osteosarcoma in com-bination with an adenocarcinoma.

Clinical Report

A woman of 76 sought advice regarding a painlessswelling in the left breast. She stated that it hadbeen present for four months, and claimed thatshe had had no previous trouble with the breasts.On examination she was a rather obese elderly

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A composite malignant tumour of the elderly female breast

Fig. 1 Clinical photograph of the breast tumour. Fig. 4 The opened cystic tumour. The two pedun-The pigmented lesions on the abdominal wall are culatedpolyps (the larger, arrow 1; the smaller,seborrhoeic keratoses. arrow 2), the small white sessile growths (arrow 3),

and the rigid, hard lining to the cyst (arrow 4) areclearly seen.

SEMILUNAR FOLD

SG4WVOUS ETHEL/CVW

OSTOWNIC SARCOMWArNOCACaNOMWAINTRAO6'Cr CARCIVOMAf

POLYPOID AqOjE-CT/J)vaA7Pf*E OSTEOP&IAMAr/VE SAROMA

.SOa4MOU4r R4P/OlMAAS

Fig. 2 Key diagram of the opened cystic tumour.

wALL or cysT

ADENOCARCINOMA

f/BROAOENOS/S

iNEV,D CYSTS

OS7EOGEN/C SARCOMA

Fig. 3 Key diagram of the larger of the twopedunculatedpolyps.

woman. The left breast was the site of a multi-nodular mass about 12-5 x 7-6 cm situatedbehind the nipple and extending over to themedial quadrant (Fig. 1). Lymph nodes were notpalpable in the axillae or supraclavicular fossae.The overlying skin was adherent to the swellingand showed a bluish discoloration. The mass was

at the apex of a rather pendulous breast andwasfreely mobile on the chest wall.She had gravitational ulcers on both ankles

and a mild degree of uterine prolapse but wasotherwise apparently fit. A chest radiographshowed slight cardiac enlargement and congestivechanges in the lungs but no evidence ofmetastases.

OPERATIONA left simple mastectomy without axillary dis-section was performed on 30 October 1968.The postoperative course was uneventful, the

wound healing satisfactorily, and the patientwas discharged on the 25th postoperative day.When seen for follow up at three and six

months there was no evidence of recurrence anda radiograph showed no chest metastases.

Pathology

MACROSCOPIC APPEARANCEThe mass in the amputated breast proved to bea tense cystic tumour 10-0 x 7-5 x 5 0 cm. Oncutting into the tumour 200 ml of dark brownviscous fluid escaped, revealing a unilocular cyst,partitioned by a narrow semilunar fold on itsposterior wall. The cyst failed to collapse, havinga rigid wall which was extensively calcified. Twopedunculated polypoid nodules with greyish-whiteirregular surfaces projected into the cavity of thecyst; the larger, 3 5 x 1-5 x 1 3 cm, hanging fromthe roof, the smaller, 2-0 x 1-8 x 1-7 cm, arisingfrom the medial floor (Figs. 2 and 3). Bothnodules were bony hard in consistency and im-possible to section with a knife. In addition fivesmall, white sessile cauliflower growths werescattered on the cyst lining ranging in size froma few millimetres to 1-0 cm in diameter. The

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D. M. Wayte, J. B. Stewart, and C. G. McKenzie

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Fig. 5 Osteogenic sarcoma composing the structureof the smaller pedunculated polyp. Haematoxylinand eosin x 40.

Fig. 6 Multinueleated-giant- cll-within theosteosarcoma. Haematoxylin and eosin x 400.

remainder of the cyst liningwas smooth, whiteandglistening (Fig. 4). Contiguous with the upperlateral pole of the cyst there was a solid area offibrofatty breast tissue. Lymph nodes were notidentified in the specimen.Numerous blocks were prepared from the cyst

wall, the intracystic projections, and surroundingbreast parenchyma.

METHODSTissue was fixed in 10% neutral formol-saline.Decalcification of the bony areas was carried outin 5% nitric acid (stabilized with 01% urea).Sections were stained with haematoxylin andeosin. The following special stains were alsoutilized: Masson's trichrome, Gordon and Sweet'smethod for reticulin, alcian blue for mucopoly-saccharides, and Hale's colloidal iron techniquesfor acid mucopolysaccharides (with and withouthyaluronidase).

MICROSCOPIC APPEARANCEThe main feature of the histology of this unusualbreast tumour was the varied mixture of tissue itcontained.The smaller of the intracystic bony nodules was

composed entirely of malignant tumour histo-logically indistinguishable from an osteosarcomaof a well differentiated type (Fig. 5). The base ofthe nodule consisted of squamous epitheliumwith an abrupt transition to a cellular stromacomposed of a mixture of spindle and polyhedralcells with hyperchromatic nuclei. Mitotic figureswere fairly numerous. Multinucleated giant cellsof the type common in osteoclastoma wereprominent (Fig. 6) and islands of osteoid andosseous material lay uniformly throughout thestroma (Fig. 7).

Sections of the larger, downwardly projectingnodule revealed a mosaic of benign and malignanttissues (Fig. 8). The base was again formed ofregular non-keratinizing squamous epitheliummerging abruptly into a stalk composed ofmaturebone with well formed trabeculae and a benigncellular fibrous stroma (Fig. 9). Embedded in thisstalk were two foci ofundoubted adenocarcinoma.The adenocarcinoma was composed of irregularducts, some crowded 'back to back' and sharingwalls lined by a single cuboidal or columnarepithelium and solid areas of pleomorphic cellswith little intervening stroma (Fig. 10). In partsthere was an intracystic papillary structure (Fig.11). Mitotic figures were numerous. Surroundingthis carcinoma were islands of mature squamousepithelium, a few small cysts with squamousepithelial linings, and the mature bone composingthe main tissue of the nodule (Fig. 12). At theapex, however, there was an abrupt transitionfrom benign-looking bone to malignant osteo-formative tissue, the appearances being identical



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Fig. 7 Osteogenic sarcoma. Osteoid, bone, andmitotic activity are clearly seen. Haematoxylin andeosin x 400.

Fig. 8 An area of the larger pedunculated polypdisplaying squamous epithelium, bone, andadenocarcinoma. Haematoxylin and eosin x 40.

Fig. 9 Surface squamous epithelium and bone ofthe larger pedunculated polyp. Haematoxylin andeosin x 140.



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.- zi;_I.- #

Fig. 10 Infiltrating adenocarcinoma and an area ofbone within the larger pedunculated polyp.Haematoxylin and eosin x 140.

with the sarcoma in the companion but smallerprojection (Fig. 13).

Sections from the cyst wall revealed densefibrous tissue lined by non-keratinizing squamousepithelium which was continuous with the basesof the tumour projections and which becamehyperplastic and papillomatous to form the smallcauliflower excrescences noted in the grossspecimen (Fig. 14). Beneath the lining epitheliumwere thin plaques of calcification and a fewfragments of benign osteoid.The tissue immediately surrounding the cyst

consisted of compressed atrophic parenchyma.The dense fibrofatty area adjacent to the cystshowed florid fibrocystic disease-dilated ductslined by hyperplastic epithelium (mild epithe-liosis), duct papillomatosis, apocrine metaplasia,fibrosis, and chronic inflammatory cell infiltration.There was no microscopic evidence to suggest thatthe cystic tumour had originated in a fibro-adenoma. There was no malignant tissue in thebreast parenchyma outside the cystic tumour.

Discussion

Early in foetal life the parenchyma of the breast

develops as a result of downward growth offinger-like epithelial processes from the overlyingectoderm. As the epithelial tracts progress andproliferate each extension becomes closely in-vested by a specialized connective tissue. This,special relationship between epithelium andmesenchyme can be seen during all the hormonalvicissitudes of mammary tissue and may also bedemonstrated in the common benign patholo-gical conditions of the breast.

Fibroadenosis with its multiplicity of micro-scopic features is undoubtedly the commonestpathological lesion of the human female breast.Occasionally cyst formation may predominate.The epithelial lining of such cysts most commonlyundergoes pressure atrophy but on occasionproliferation, papillary formation, and evenintracystic carcinoma can be seen. That a relation-ship exists between fibroadenosis and breastcarcinoma is now accepted by most authorities(Davis, Simons, and Davis, 1964) but any suchrelationship between fibroadenosis and the lesscommon breast sarcoma has not been defined.However, a distinct relationship between thefibroadenoma and sarcoma is definintely estab-lished (Curran and Dodge, 1962).A fibroadenoma,most commonly arising in the breast of the youngadult woman, may be considered as a local area



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Fig. 11 Another area ofadenocarcinoma displayingpapillary formation. Haematoxylin and eosin x 40.

Fig. 12 The bone trabeculae composing the mainstructure of the larger pedunculated polyp.Haematoxylin and eosin x 140.

ofmammary dysplasis which is possibly hormonedependent. When seen in the older woman suchgrowths are more likely to represent but onevariant of a generalized picture of fibroadenosisand therefore separation between fibroadenomaand fibroadenosis is less clearly possible in thisage group.

Giant fibroadenomas (benign cystosarcomaphyllodes) present most commonly in the elderlyfemale. A history of recent rapid growth is oftengiven by the patient and such a statement oftenresults in consideration of a malignant processalthough on microscopic examination the majorityof such tumours have a benign structure (Ober-man, 1965a). The great percentage of giantfibroadenomas have a solid macroscopic appear-ance with only occasional clefts separating theconstituent lobules but occasionally the tumourassumes a cystic form, the intra-canalicular pro-jections of stroma and epithelium remaining aspolypoidal projections into the cystic cavity.That the stroma of a fibroadenoma may under-

go metaplasia to form heterologous tissue is wellknown (Robb and Macfarlane, 1958). Less wellknown is the fact that in rare instances theepithelial component may also undergo meta-plasia to that of a squamous type (Salm, 1957;Willis, 1962).Tumours of the canine (Fidler and Brodey,

1967) and feline breast (Schmidt and Langham,1967) often show metaplasia of the stromaresulting in the formation of bone and cartilage(Allen, 1940; Willis, 1967). Such a phenomenonis rare in the human breast and when seen involvesthe stroma of benign or malignant fibroadenomas(Rottino and Howley, 1945; Willis, 1967). Thehistogenesis of osseous metaplasia in closeapproximation to epithelial tissues is poorlyunderstood (Collins and Curran, 1959) but maybe seen in the gastrointestinal and genitourinarytracts (Pang, 1958) and in certain tumours of theskin and salivary glands (Yates and Paget, 1952).At these various sites it has been proposed thatthe epithelium acts as an 'organizer' in stimulatingthe surrounding mesenchymal cells to lay downbone. Experiments with transplanted urinary(Constance,1954) and gallbladder epithelium haveresulted in the formation of bone within themesenchyme adjacent to the transplant (Huggins,1931). In an attempt to relate this process toparticular epithelial cells, Azzopardi and Smith(1959), in their study of salivary gland neoplasms,proposed that the myoepithelial cell was res-ponsible for the production of the connectivetissue mucins in which bone could be formed.

Occasionally giant intracanalicular fibro-adenomas are found to be histologically malig-nant (malignant cystosarcoma phyllodes), themesenchymal component being most commonlyimplicated to form a spindle cell sarcoma.Stewart (1950) pointed out that 'a very smallnumber of these tumours develop bizarre struc-



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Fig. 13.

Fig. 13 Osteoid formation within an area ofZ ~~~~osteosarcoma seen in the larger polyp. Note the

' J } .;mitoticfigure. Haematoxylin and eosin 400.

, ,.,Fig. 14 The abundant squamous epithelium composing the small sessile 'cauliflower-like' excrescences.

tx'* Note the bone formation and the vascular channelsin the underlying cyst wall. Haemzatoxylin and

. eosin x 40.

tural patterns with the formation of atypical boneand cartilage' while Willis (1959) considers that

j ~~~ Such metaplastic tissue may be malignant andform osteosarcomas, chondrosarcomas, and

Osteoclastomas.@t:lThe classification of breast sarcoma is a con-Q' '!' fusing topic (Norris and Taylor, 1968). All authors

accept the so-called 'pure' sarcomas as definite$,;5VV entities but it is in regard to the sarcomas con

tamning an epithelial component where disagree-ment exists. Botham, McDonald, and Clagett(1958) considered that lesions containing anepithelial component intermixed with a richlycellular stroma should be excluded, while other

)* workers (Oberman, 1965b; Lattes 1967) con-e e.4;sidered that carcinomas associated with malig

... nant metaplasia of their surrounding stroma(composite tumours or combined tumours)

Fig.14- should also be excluded from any series of breast



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sarcoma. However, the majority of workers inthis field accept the possibility of intermixture ofcomponents in mammary gland neoplasms, and,although there is no clear uniformity, thefollowing categories of breast sarcoma arecommonly listed:

'PURE' SARCOMA

These are (1) sarcomas not specifically related tomammary tissue, eg, malignant lymphoma; (2)sarcomas arising from general breast mesen-chyme, eg, liposarcoma and haemangiosarcoma;(3) sarcomas not appearing to arise from fibro-adenomas and having a uniform structure.

COMPOSITE TUMOURS

Sarcomas arising from a fibroadenoma, eg,malignant cystosarcoma phyllodes, are oftencomposite tumours.

Certain authorities clearly separate sarcomas

of the malignant cystosarcoma phyllodes typefrom the diffuse pure sarcomas not seen to arisefrom a fibroadenoma, for the former rarelymetastasizes, thereby differing from the moreaggressive pure sarcoma. However, in a number ofinstances it may not be possible to demonstratesuch an origin owing to the destructive andinvasive nature of the neoplasm (Fawcett, 1967).The great majority of sarcomas of the breast

occur in elderly women. They are extremely rare(Botham et al, 1958; Hill and Stout, 1942) and in a10-year period formed only 0 9% of all malignantbreast tumours seen at one hospital (Curran andDodge, 1962), and stromal sarcomas accountedfor only 0-6% of 5,458 malignant breast tumoursin the series of Kennedy and Biggart (1967). Inregard to the sarcomas which have undergonemetaplasia, the case described by Jermstrom et al(1963) was the only osteosarcoma in 3,309malignant neoplasms of the breast collected in18 years. It is clear, therefore, that osteosarcomaof the breast is a distinct rarity, and some authors(Lattes, 1967) do not accept such an entity andregard the examples of bone and cartilage formedby malignant tumours of the breast as probablycarcinomas with osseous and cartilaginous meta-plasia. Smith and Taylor (1969), in their recentseries of 35 cases from the files of the ArmedForces Institute of Pathology, regard most of theheterologous bone and cartilage seen in breasttumours to arise from stromal metaplasia but alsoaccept that certain adenocarcinoma cells mayundergo direct transition to form bone- andcartilage-forming cells. Willis (1959) regards themajority of predominantly cartilaginous, bonyand osteoclastic mammary tumours as meta-plastic variants of the 'cystosarcoma' group andadvocates their segregation as a subgroup ofmammary sarcoma because of their relativelyfrequent malignancy.

When an adenocarcinoma develops jointly witha metaplastic breast sarcoma a most bizarrepicture (Willis, 1967), as is seen in our presentcase, results. This intermixture of an epithelialand mesenchymal neoplasm must undoubtedlyraise many difficulties in interpretation and inclassification. It should be pointed out, however,that such composite or mixed malignant tumoursare commonly seen in the canine and feline breastand metastases of both malignant elements havebeen described.

Hill and Stout (1942) postulated that there werethree possible ways for a composite malignanttumour to develop: (1) malignant transformationof an epithelial and a mesenchymal componentof a teratoma; (2) a primary carcinoma incitingthe surrounding stroma to malignancy; (3) amalignant stroma inciting the adjacent epithelium.

Possibly a fourth postulate should be added tothe above list which would explain the multiplechanges seen in our present case. As indicatedearlier in this discussion, a close associationbetween epithelium and mesenchyme of thebreast definitely exists and it seems not unreason-able to consider the possibility of an inciting agentinducing metaplasia and neoplasia of both com-ponents simultaneously.The prognosis ofmammary tumours containing

osteoid tissue remains conjectural due to thesmall number of cases seen in any one series.Rottino and Howley (1945) pointed out the dangerof incomplete removal by local enucleationtechniques but considered that simple mastectomywas normally adequate because of the very lowincidence of lymph node metastases.

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Azzopardi, J. G., and Smith, 0. D. (1959). Salivary gland tumoursand their mucins. J. Path. Bact., 77, 313-140.

Botham, R. J., McDonald, J. R., and Clagett, 0. T. (1958).Sarcoma of the mammary gland. Surg. Gynec. Obstet.,107,55-61.

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Constance, T. J. (1954). Localised myositis ossificans. J. Path.Bact., 68, 381-385.

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